Proximate and elemental composition of leaf, , root and peel of Hypoxis hemerocallidea: A Southern African multipurpose medicinal

Gloria Aderonke Otunola* and Anthony Jide Afolayan Medicinal and Economic Development (MPED) Research Centre, Department of Botany, University of Fort Hare, Alice, South

Abstract: Hypoxis hemerocallidea also known as African potato is a medicinal plant widely distributed in Southern Africa, which has enjoyed long usage as a traditional multipurpose herbal medicine. This study evaluated the leaf, corm, peel and root of H. hemerocallidea for their nutritional attributes. Crude protein was highest in leaf (5.56%), followed by peel (2.79%), root (2.30%) and corm (1.79%) respectively. Crude fat ranged from 0.40% in root to 1.88% in leaf, while ash and acid detergent fibre (ADF) were highest in corm (16.77% and 49.75%) and lowest in root (3.20% and 5.46%) respectively. Neutral detergent fibre (NDF) was highest in leaf (55.47%), followed by corm (52.38%), peel (35.23%) and root (10.51%); while total carbohydrate calculated as non-fibre carbohydrate was highest in the root. The corm had the highest content (P<0.05) of calcium, zinc, copper and manganese, the root exhibited the highest content of magnesium, potassium and iron, while sodium and phosphorus content was highest in the leaf. The study revealed that H. hemerocallidea leaf, corm, peel and root are good sources of nutrients and minerals for humans and animals. This implies that the plant as a whole could be more effective therapeuticaly than the corm alone.

Keywords: Hypoxis hemerocallidea, nutritional attributes, medicinal plant, mineral composition.

INTRODUCTION herbaceous corm/tuberous plant with yellow star-shaped in early summer, mid and late spring. It grows Traditional medicine plays a critical role in the health care well in semi-shade and direct sun, and prefers medium delivery system of the general population in most parts of levels of water. The leaves are green in spring, summer Africa. This is very true of South Africa because of the and autumn with rough thick hairs (Russell et al., 1987). increased burden of chronic and communicable diseases such as diabetes, cardiovascular diseases, obesity and H. hemerocallidea corm has been used by traditional HIV/AIDS. In recent times, there has been an increase in healers in southern Africa for the treatment and the study of plant foods with nutraceutical, management of various ailments including tuberculosis, pharmaceutical, nutritional and functional properties. diabetes, cancer, urinary tract infections, prostrate Many wild plants with multi-functional properties are hypertrophy and testicular tumors as well as an immune now gaining recognition and usage. H. hemerocallidea is booster in HIV/AIDS. one of such plants which has recently become a subject of scientific study and is potentially an important Other uses of the plant in the treatment of rheumatoid breakthrough in the field of medicinal plants. arthritis, endometriosis and premenstrual syndrome, mental disorders, impotence, anti-inflammation and as a Also known as African potato, Hypoxis hemerocallidea is worm expeller have been documented (Ojewole 2006, an African medicinal plant widely distributed in South Ojewole et al., 2006; Steenkamp et al., 2006; Nair et al., Africa, which has enjoyed long usage as a traditional 2007; Singh 2007). Traditionally, the are chopped herbal medicine. The plant is characterized by strap-like into pieces, boiled for about twenty minutes and the leaves, bright yellow, star-shaped flowers and a tuberous decoction consumed orally. root stock or corm erroneously referred to as African potato because of its shape (Van Wyk et al., 2002; Owira Extensive studies on the pharmacological, phytochemical, and Ojewole, 2009). H. hemerocallidea grows in the open hypoglycaemic, antioxidant, anticancer, and anti-diabetic grass and woodlands and is widespread in the Eastern properties as well as the β-sitosterol, monoterpene Cape, Free State, Mpumalanga, Gauteng and Limpopo glycosides and zeatin content of H. hemerocallidea have Provinces of South Africa. It also grows in Botswana, been reported (Pegel 1973; Van Staden 1981; Drewes et Lesotho, Mozambique and Swaziland. al., 1984; Musabayane et al., 2005; Boukes et al., 2008). However, there is a dearth in the literature on the Hypoxis hemerocallidea (fig. 1) is a hardy, perennial and proximate and elemental composition of the different *Corresponding author: e-mail: [email protected] parts of the plant. This study was therefore conducted to Pak. J. Pharm. Sci., Vol.32, No.2, March 2019, pp.535-539 535 Proximate and elemental composition of leaf, corm, root and peel of Hypoxis hemerocallidea: A Southern African assess the nutritional and elemental composition as well (NDF) and acid detergent fibre (ADF). NDF varied as their variations in different parts of H. hemerocallidea. significantly among the various parts with the root having the lowest value of 10.51%, peels 35.23, corm 52.38% MATERIALS AND METHODS and leaf 55.47%. These values were significantly different at P < 0.05. ADF content on the other hand was in the H. hemerocallidea whole plant was collected from the order corm > leaf > peels > roots. Carbohydrate was wild in Alice in the Eastern Cape Province of South calculated as non-fibre carbohydrate (NFC) by subtracting Africa. The plant was identified by Prof DS Grierson of the sum of crude protein, NDF-ADF, crude fat and ash the Department of Botany and voucher specimen from 100. NFC was highest in the roots (83.59%), (Otun.2013/04) was deposited at the Giffen herbarium of followed by the peels (51.04%), while leaf and corm the University of Fort Hare. The plant was separated into contents were 22.24% and 28.06% respectively. leaves, corm, peels and roots; each part was dried in the oven at 45ºC for 72h, then milled into fine powder and stored in airtight glass bottles at 4ºC till needed for analysis. All reagents used in the study were of analytical grade.

Proximate analysis Powdered H. hemerocallidea leaf, corm, peels and roots were assessed for crude protein (CP), crude fat (CF), ash and crude fibre on 100% dry matter (DM) basis according to methods described by AOAC (2000). Neutral detergent fibre (NDF) and acid detergent fibre (ADF) were determined according to the methods of Soest and Robertson (1980). Total carbohydrate (non-fibre-NFC) was calculated as 100- [(NDF-ADF-CP)+CP+Fat+Ash]. All determinations were in triplicates.

Mineral elements analysis Fig. 1: Hypoxis hemerocallidea Fisch. The macro and micro elements of the various parts of H. hemerocallidea were determined as described by Mineral analysis of leaf, corm, peel and root of H. Okalebo (2002) using Inductively Coupled Plasma hemerocallidea (table 2) showed that the Ca, Zn, Cu and Optical Emission Spectrometry (ICP-OES, Varian 710- Mn content of the corm was significantly higher ES Series). All determinations were in triplicates. compared to other parts of the plant. The roots exhibited a significantly high Mg, K, K:Ca:Mg ratio and Fe content, STATISTICAL ANALYSIS while the leaf was significantly high in Na and P. There were no significant (P > 0.05) differences in the values for Results were expressed as means ± standard deviation of Mg in leaf and peel; and corm and root; P in the root, three determinations. One-way analysis of variance was corm and peel; Cu in peel and root; Mn in leaf and corm used to determine the differences of means among the and Zn in leaf and root. samples. A significant difference was considered at the level of P<0.05. All analyses were carried out using DISCUSSION MINITAB (Student Version 12 for Windows) Software. Plants play significant roles in maintaining health and are RESULTS valuable components of the diet and folkloric medicines. These nutritional and healing properties of plants are Results for the proximate composition of leaf, corm, stem attributed to their chemical composition. According to and peel of H. Hemerocallidea is presented in Table 1. Pandey (2006), evaluating the proximate and nutritional Protein content varied significantly in all the parts and contents of medicinal plants can help to understand the ranged from 2.30% to 5.66% in the roots and leaves therapeutic properties of these plant species. respectively. Crude fat content was significantly low in all the samples; and followed the order leaf > corm > peel > Crude protein content of the leaf of H. hemerocallidea root. Ash content was generally high and varied which was the highest of the four parts investigated, was significantly (P < 0.05) in the different parts of the plant. still relatively low. According to NRC (1989), crude The corm had the highest content of 16%, while the leaf, protein less than 20% is an indication of low protein peel and roots had 14.85, 10.08 and 3.20 respectively. value. However, despite the low protein content in the Fibre content was determined as neutral detergent fibre parts investigated, each part can contribute to the protein 536 Pak. J. Pharm. Sci., Vol.32, No.2, March 2019, pp.535-539 Gloria A Otunola et al

Table 1: Proximate composition of leaf, corm, peel and root of H. hemerocallidea

Parameters (%) Leaf Corm Peel Root Crude Protein 5.56±0.10a 1.79±0.13b 2.79±0.11c 2.30±0.08d Crude Fibre 55.47±0.20a 52.38±0.02b 35.23±0.07c 10.51±0.15d Crude Fat 1.88±0.02a 1.00±0.02b 0.86±0.03c 0.40±0.01d Ash 14.85±0.05a 16.77±0.80b 10.08±0.01c 3.20±0.05d ADF 33.84±0.69a 49.75±0.60b 31.80±0.01c 5.46±0.12d NDF 55.47±0.20a 52.38±0.02a 35.23±0.07c 10.51±0.15d Carbohydrate (NFC) 22.24±0.24a 28.06±0.07b 51.04±0.02c 83.59±0.25d *Values are means n=3, ± SD. Values along the same row with different superscripts are statistically different (P < 0.05). ADF-acid detergent fibre; NDF-neutral detergent fibre; NFC- non-fibre carbohydrate.

Table 2: Elemental content of leaf, corm, peel and root of H. hemerocallidea

Elements (mg/100g) Leaf Corm Peel Root Macro elements Ca 1.59±0.02a 1.72±0.10b 0.59±0.03c 0.97±0.01d Mg 0.10±0.02a 0.17±0.02b 0.10±0.02a 0.19±0.02bc K 1.93±0.02a 0.90±0.50b 0.67±0.01c 2.54±0.14d Na 1.14±0.06a 0.14±0.02b 0.06±0.01c 0.65±0.02d K/Ca+Mg 0.56±0.08a 0.23±0.10b 0.45±0.01c 1.01±0.01d Micro elements P 0.07±0.02a 0.03±0.01b 0.03±0.01b 0.03±0.01b Zn 18. 00±1.00a 45.00±2.00b 30.67±0.58c 16.00±1.00a Cu 8.00±1.00a 16.00±1.00b 9.00±0.08c 9.00±1.00c Mn 96.67±7.64a 96.67±7.64a 41.00±1.00b 63.00±1.00c Fe 901.0±1.00 1122.0±2.00 16.0±1.00 2315±2.00 *Values are means n=3, ± SD. Values along the same row with different superscripts are statistically different (P < 0.05). requirements of the body. The protein content for the leaf component of plants and predictor for voluntary intake also compared favourably with reports for most medicinal because it provides bulk or fill (Ferguson 2013). In this plants such as Corianderum sativum (3.5%), Hibiscus study, the low NDF value of the root, implies that it will sabdariffa (1.8%) and Trigonela foenum-graecum (5.4%) be easily digested and thus suggests the possibility of its respectively (Ereifej et al., 2012); though higher values inclusion in diets. Acid detergent fibre (ADF) consists of (23.36%) have been reported in Ipomea hederacae seeds the least digestible plant components and are inversely (Zia-Ul-Haq et al., 2012). related to digestibility. Low ADF values are higher in energy; this implies that the root is likely to increase the The low crude fat content of all the parts investigated energy value of any diet it is added to compared with the indicates that H. hemerocallidea is a poor source of fat. A peel, corm and leaf. Dietary fibre has been reported to aid study of the fatty acid profile of the little fat present may absorption of minerals and reduce absorption of prove beneficial as they may contain valuable essential cholesterol (Aliyu et al., 2009). Results for non-fibre fatty acids. According to Egwuche et al. (2011), most carbohydrate (NFC) revealed that the root had the highest vegetables are poor sources of lipids. This may be useful carbohydrate content and compared favourably with other for individuals on weight-reducing diets, or those medicinal plants (Ajayi and Ojelere 2013; Aliyu et al., suffering from hyperlipidemia, obesity and cardiovascular 2009). complications. The importance of dietary minerals are well documented. Ash content is usually taken as an indication of the The high calcium content of the corm and leaf of H. mineral content of a sample. The high ash content hemerocallidea observed in this study, suggests that these observed for corm, leaf and stem compared favourably two parts could supply or augment the necessary calcium with reports for other medicinal plants such as Origano needed for mediating vascular contraction, nerve-impulse majorana and Salvia officinalis (Ereifej et al., 2012) and transmission and glandular secretions. Potassium content indicate the high mineral content of the plant. was noticeably higher in all parts of the plant compared to sodium content. This means a low Na/K ratio which has Neutral detergent fibre (NDF) is considered to be the been reported to be good for the maintainance of acid- entire fibre fraction of a feed. It is the structural base balance and lower incidences of hypertension (Choi Pak. J. Pharm. Sci., Vol.32, No.2, March 2019, pp.535-539 537 Proximate and elemental composition of leaf, corm, root and peel of Hypoxis hemerocallidea: A Southern African et al., 2011; Sarega et al., 2012). Magnesium is important and elemental contents. Further studies to assess the in fighting heart disease, stroke and in cell repair biological functions of each part is on-going. (Agunbiade et al., 2012). The presence of Magnesium in the leaf, corm, peel and root of H. hemerocallidea could ACKNOWLEDGEMENTS account for the use of the plant in the treatment of cardiovascular diseases. Magnesium (Mg) and calcium This study was supported by the National Research (Ca) antagonize each other in (re)absorption, Foundation (NRF) South Africa; and Govan Mbeki inflammation and many other physiological activities. Research Development Centre (GMRDC), University of The low K/Ca/Mg ratio observed in this study implies that Fort Hare, South Africa. dietary magnesium, calcium, zinc and phosphorus bioavailability will not be compromised and there will be REFERENCES reduced risk of mortality (Dai et al., 2013). Ahmed D and Chaudhary MA (2009). Medicinal and Iron is a component of myoglobin and haemoglobin nutritional aspects of various trace metals determined needed for transport of oxygen and carbon dioxide in Ajuga bracteosa. J. Appl. Sci. Res., 5(7): 864-869. (Ahmed and Chaudhary 2009; Kamshilov and Agunbiade OS, Ojezele OM, Ojezele JO and Ajayi AY Zaprudnova 2009). The high amount of iron found in the (2012). Hypoglycaemic activity of commelina africana root, corm and leaf of H. hemerocallidea indicates that and ageratum conyzoides in relation to their mineral the specie could be a very good source of iron and could composition Afr. Health. Sci., 12(2): 198-203. therefore be used to overcome iron deficiency. Ajayi IA and Ojelere OO (2013). Chemical composition of ten medicinal plant seeds from South-West . Copper, zinc and manganese are essential trace elements Adv. Life Sci. Tech., 10, (online). needed in minute amounts by the human body for Aliyu AB, Musa AM, Sallau MS and Oyewale AO important biochemical functions. These three elements (2009). Proximate composition, mineral elements and play important roles in reproduction and are closely anti-nutritional factors of mannii N.E.Br. interelated (Osredkar and Sustar 2011; Ooi et al., 2012). Asclepiadaceae). Trend. Appl. Sci. Res., 4: 68-72. H. hemerocallidea is a very good source of Zn, Cu and Association of Official Analytical Chemists (2000). Mn and their presence could account for the Official Methods of Analysis of AOAC International multifunctional medicinal uses of the plant especially in 17th Ed; AOAC International, Gaithersbury, MD, USA. body building, pro-fertility and boosting of the immune Baker DD, Chu M, Oza U and Rajgarhia V (2007). The system. value of natural products to future pharmaceutical The current use of the corm of H. Hermerocallidea does discovery. Nat. Prod. Rep., 24(6): 1225-44. not provide for its sustainable use since the use of the Boukes GJ, Van de Venter M and Oosthuizen V (2008). root, corm and whole-plant harvesting is more destructive Quantitative and qualitative analysis of sterols/sterolins to medicinal plants and results in resource exhaustion and and hypoxoside contents of three Hypoxis (African even species extinction than collecting their leaves and potato) spp. Afr. J. Biotechnol., 7(11): 1624-1629. flowers or buds (Baker et al., 2007; Chen et al., 2016). To Chen S-L, Yu H, Luo H-M, Wu Q, Li C-F and Steinmetz this end, the sustainable use of H. Hermerocallidea A (2016). Conservation and sustainable use of should be considered by using the leaves as a remedy and medicinal plants: Problems, progress and prospects. alternative to the corm. Chinese Medicine, 11: 37. Choi M, Scholl UI, Yue P, Bjorklund P, Zhao B, Nelson- CONCLUSION Williams C and Ji B (2011). K+ channel mutations in adrenal aldosterone-producing adenomas and H. hemerocallidea corm is well known for its hereditary hypertension. Science, 331: 768-772. multipurpose therapeutic functions. This study has shown Dai Q, Shu XO, Deng X, Xiang YB, Li H, Yang G, that the leaf, peel and root of the plant also possess high Shrubsole MJ and Ji B (2013). Modifying effect of nutritional and mineral components. The presence of calcium/magnesium intake ratio and mortality: A these nutrients and essential trace elements in this plant population-based cohort study. Brit. Med. J. Open., may readily account for most of the therapeutic 3(2): e002111. properties. Therefore, all parts of the plant could be used Drewes SE, Elliot E, Khan E, Dhlamini JTB and Gcumisa for animal nutrition, tea production or dietary MSS (2008). Hypoxis hemerocallidea – not merely a supplementations. This indicates that the various parts cure for benign prostate hyperplasia. J. could also be integrated as functional foods into the diet. Ethnopharmacol., 119: 593-598. Whereas the corm alone is used traditionally for Egwuche RU, Odetola AA and Erukainure OL (2011). medicinal purposes, this study reveals that the whole plant Preliminary investigation into the chemical properties could be more effective therapeuticaly and that the leaves of Peperomia pellucida. L. Res. J. Phytochem., 5: 48- compare favourably with the corm in terms of nutrient 53. 538 Pak. J. Pharm. Sci., Vol.32, No.2, March 2019, pp.535-539 Gloria A Otunola et al

Ereifej K, Ranya E, Taha R, Ali MA and Muhammad HA Russell GE, Welman WG, Reitief E, Immelman KL, (2012). Minerals, proximate composition and their Germishuizen G, Pienaar BJ, Van Wyk M and correlations of medicinal plants from Jordan. J. Med. Nicholas A (1987). List of species of southern African Plant. Res., 6 (47): 5757-5762. plants. Memoirs Botanical Surv. SA., 2(1-2): 1-152(pt. Ferguson J.D (2013). Carbohydrate Fractions in Dairy 1), 1-270(pt. 2). Rations. In: Carbohydrates in Rations: http://research. Sarega N, Iqbal S, Chan WK and Ismail M (2012). vet.upenn.edu/Default.aspx?alias=research.vet.upenn.e Assessment of nutritional and mineral composition of du/dairynutrition. different parts of Schismatoglottis bauensis. J. Med. Kamshilov IM and Zaprudnova RA (2009). Interspecies Plant Res., 6(9): 1576-1580. differences of haemoglobin buffer properties and of ion Singh Y (2007). Hypoxis () in Southern environment in some freshwater fish. J. Evol. Biochem. Africa: Taxonomic notes. South Afr. J. Bot., 73: 360- Physiol., 45(2): 242-244. 365. Musabayane CT, Gondwe MM, Shode FO and Ojewole Steenkamp V, Gouws MC, Gulumian M, Elgorashi EE JAO (2005). Hypoglycaemic effects of Hypoxis and Van Staden J (2006). Studies on antibacterial, anti- hemerocallidea (Fisch. and C. A. Mey.) inflammatory and antioxidant activity of herbal [Hypoxidaceae] corm ethanolic extract in rats. remedies used in the treatment of benign prostatic Presented at Society for Endocrinology BES London, hyperplasia. J. Ethnopharmacol., 103: 71-75. UK. Endocrine Abstracts., 10: 34. Van Soest PJ and Robertson JB (1980). Systems of Nair VPD, Dairam A, Agbonon A, Arnason JT, Foster analysis for evaluating fibrous feeds. In: BC and Kanfer I (2007a). Investigation of the Standardization of Analytical Methodology in Feeds antioxidant activity of African potato (Hypoxis (Pigden W.; Balch CC & Graham M eds.), hemerocallidea) corm. J. Agric. Food. Chem., 55: International Research Development Center, Ottawa, 1707-1711. Canada, pp.49-60. National Research Council (1989). Committee on Dietary Van Staden J (1981). Constituents of H. rooperi a Allowances: Recommended Dietary Allowances 1989, valuable plant in South Africa. Deutsche Apothecary. 10th edn, National Academy of Science Press, ZTG, 33: 460-464. Chemical Abstract CA95 (19), Washington DC, USA. 165595x. Ojewole JAO (2006). Antinociceptive, anti-inflammatory, Van Wyk BE, Van Outshoorn B, Gericke N (2002). and antidiabetic properties of Hypoxis hemerocallidea Medicinal plants of South Africa, 2nd edn. Briza Fisch. & C.A. Mey (Hypoxidaceae) corm [African Publications. Pretoria, pp.156-157. potato] aqueous extracts in mice and rats. J. Venugopala KN, Rashmi V and Odhav B (2013). Review Ethnopharmacol., 103: 126-134. on Natural Coumarin Lead Compounds for Their Ojewole JA, Kamadyaapa DR and Musabayane CT Pharmacological Activity. Bio Med Res. Intern., (2006). Some in vitro and in vivo cardiovascular effects Article ID 963248, 14 pages, 2013. of Hypoxis hemerocallidea Fisch & CA Mey doi:10.1155/2013/963248 (Hypoxidaceae) corm (African Potato) aqueous extract Zia-Ul-Haq M, Riaz M and De Feo V (2012). Ipomea in experimental animal models. Cardiovasc J. South herdacea Jacq: A medicinal herb with promising health Africa., 17(4):166-171. benefits. Molecule, 17: 13132-13145. Okalebo JR, Gathua W and Woomer PL (2002). Laboratory methods of soil and plant analysis: A working manual. 2nd edn. TSBF-CIAT and SACRED Africa, Nairobi, Kenya. Ooi DJ, Iqbal S and Ismail M (2012). Proximate composition, Nutritional Attributes and Mineral composition of Peperomia pellucida L. (Ketumpangan Air) grown in Malaysia. Molecule, 17: 11139-11145. Osredkar J and Sustar N (2011). Copper and zinc: Biological role and significance of copper/zinc imbalance. J. Clin. Toxicol., S3: 001. Owira PMO and Ojewole JA (2009). African potato (Hypoxis hemerocallidea corm): A plant medicine for Modern and 21st century Disease of Mankind? A review. Phytother. Res., 23(2): 147-152. Pandey MAB, Abidi S and Singh RP (2006). Nutritional evaluation of leafy vegetables Paratha. J. Human. Ecol., 19: 155-156.

Pak. J. Pharm. Sci., Vol.32, No.2, March 2019, pp.535-539 539